Journal Article

High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species

Rosenthal, Gil G, Schumer, Molly, Powell, Daniel L, Dresner, Rebecca, Cui, Rongfeng, Andolfatto, Peter

2014

Overview

Hybridization is increasingly being recognized as a common process in both animal and plant species. Negative epistatic interactions between genes from different parental genomes decrease the fitness of hybrids and can limit gene flow between species. However, little is known about the number and genome-wide distribution of genetic incompatibilities separating species. To detect interacting genes, we perform a high-resolution genome scan for linkage disequilibrium between unlinked genomic regions in naturally occurring hybrid populations of swordtail fish. We estimate that hundreds of pairs of genomic regions contribute to reproductive isolation between these species, despite them being recently diverged. Many of these incompatibilities are likely the result of natural or sexual selection on hybrids, since intrinsic isolation is known to be weak. Patterns of genomic divergence at these regions imply that genetic incompatibilities play a significant role in limiting gene flow even in young species. In nature, closely related species often interbreed to produce hybrids. However, hybrids are often less fertile or unable to compete with parent species, making them less likely to thrive in the wild. When the genomes of two different species are mixed, versions of genes that are meant to work together can become separated, which means that these genes do not work as well as they should. This reduces the hybrids' chances of survival, and a poor survival rate of hybrids is one barrier that keeps different species distinct, even though the species can interbreed. Two species of swordtail fish live in the rivers in Mexico, and although they mostly live in different stretches of these rivers, the two species interbreed to produce hybrids in the regions where they overlap. These hybrids can outnumber the parental species in these ‘hybrid zones’, but the two species have remained separate in other parts of the rivers. Though some genetic incompatibilities that might keep the species distinct have previously been suggested, it is not known how many incompatibilities there are in these fish's genomes. Schumer et al. have searched the genomes of wild hybrids between these species and found hundreds of genetic incompatibilities. These were identified by looking for species-specific pairs of genes that are found together more often than would be expected if there were no selection against hybrids. It is likely that many of these incompatibilities reduce the evolutionary fitness of the hybrid fish and Schumer et al. suggest that many could be the result of environmental pressures and the fish's mating preferences. Furthermore, Schumer et al. demonstrate that genes close to identified incompatibilities are more different between species, on average, than genes that are further away. When there is on-going interbreeding between two the species (as is the case with the swordtails), this finding is expected only if these incompatibilities reduce the hybrids' chances of finding mates or surviving. The findings of Schumer et al. demonstrate how conflicts in the genomes of two species allow these species to remain distinct even when they live in overlapping environments and frequently interbreed. Future work will investigate how these genetic incompatibilities shape the hybrid populations that are found in the wild; and which incompatibilities are caused by poor survival of the hybrids or by the fish's mating preferences selecting against the hybrids.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Chromosome Mapping - methods / Computer Simulation / Epistasis / Epistasis, Genetic / Evolution & development / Female / Fishes - genetics / Gene Flow / Gene Library / Gene mapping / genetic incompatibility / Genome / Genomes / Genomics and Evolutionary Biology / Genotype / hybrid fitness / Hybridization / Hybridization, Genetic / Hybrids / Linkage Disequilibrium / Male / Melanoma / Models, Genetic / Reproductive fitness / Reproductive isolation / Sexual selection / speciation / Species / X Chromosome / Xiphophorus birchmanni / Xiphophorus malinche